CHARACTERIZATION OF BIOACTIVE METABOLITES FROM MARINE MACROALGAE COLLECTED FROM VERAVAL COAST OF GUJARAT

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CHARACTERIZATION OF BIOACTIVE METABOLITES FROM MARINE MACROALGAE COLLECTED FROM VERAVAL COAST OF GUJARAT

Hiral P. Goswami, Jigna G. Tank * and Rohan V. Pandya

UGC-CAS Department of Biosciences, Saurashtra University, Rajkot, Gujarat, India.

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ABSTRACT: Seaweeds are potential sources of bioactive molecules. They are known to be rich sources of proteins, carbohydrates, lipids, vitamins, minerals, and other secondary metabolites. To evaluate the presence of these compounds in marine macroalgae collected from Veraval coast of Gujarat, present studies was carried out. The methanol extract of six macroalgae species (Ulva lactuca, Ulva faciata, Acanthophora dendroides, Gracilaria corticata, Padina tetrastromatica, and Cystoseira indica) was subjected to LCMS/MS analysis which suggested presence of amino acids, sugar, vitamins and phytohormones in algae extracts. The aminoacids and vitamins present in Ulva lactuca (betaine, L-methionine, L-asparagine), Ulva faciata ( L-arginine, L-proline, L-histidine, L-valine, L-Threonine, Dihydrofolic acid), Acanthophora dendroides (L-glutamic acid, L-alanine, L-serine, L-phenylalanine, L-tyrosine, nicotinic acid), Gracilaria coeticata (L-canavanine, L-isoleucine, and L-cysteine) and Padina tetrastromatica (L-Aspartic acid, L-leucine) can be utilized for the development of dietary supplements and proteinaceous food for domestic animals. The sugar present in Ulva faciata (glucosamine), Acanthophora dedroides (D-xylose, D-mannose, D-fructose), Gracilaria corticata (D-Rhamnose, fucose, D-galactose), Padina tetrastromatica (D-glucuronic acid, D-glucose, D-mannuronic acid), and Cystosera indica (arabinose, maltose) can be utilized in food products, cosmetic, gelling and thickening agents. The phytohormones present in Ulva lactuca (6-Benzylaminopurine, jasmonate), Gracilaria corticata (salicylic acid, ethylene), Padina tetrastromatica (Abscisic acid), and Cystosera indica (Indole-3 acetic acid) can be utilized in agriculture as plant growth regulators. Hence, these algae species are essential raw materials for the production of various pharmaceutical and biotechnological products.

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Keywords: Seaweeds, Bioactive metabolites, Ulva lactuca, Ulva faciata, Acanthophora dendroides, Gracilaria corticata, Padina tetrastromatica, Cystoseira indica

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INTRODUCTION: Principally, it was observed that the drugs developed from natural sources mainly come from microorganisms and terrestrial plants. However, marine organisms are the alternative sources to discover novel bioactive compounds ¹.

Secondary metabolites are organic compounds synthesized in living organisms using primary metabolites. These compounds are specific for each and every organism species within a phylogenetic group.

These secondary compounds are economically important for different pharmaceutical and biotechnological industries for synthesizing medicines, flavouring agents, thickening agents, and recreational drugs ². Marine macroalgae are natural sources of biologically active therapeutic and bioactive molecules for treating multiple diseases ^{3, 4}.

Macroalgae are the potential sources of primary metabolites and secondary metabolites which are extensively evaluated using bioassays and pharmacological studies ^{5, 6, 7}. Many secondary metabolites are produced from intermediates and end products of secondary metabolism which are grouped into terpenes, phenolics, and alkaloids ^{8, 9}. Seaweed resources such as polysaccharides, lipids, proteins, carotenoids, vitamins, sterols, enzymes, antibiotics and many other fine chemicals are used as major metabolites for human benefits ^{10, 11, 12}. Ulva fasciata contains sphingosine derivatives that have in-vivo antiviral activity ¹³. Extract of Ulva lactuca has anti-inflammatory and antitumour compounds ¹⁴. The secondary metabolites from Ulva fasciata and Hypnea musciformis enhance the bacterial clearance capability of the hemolymph of shrimp and Penaeus monodon ¹⁵.

Portieria hornemannii contains halogenated monoterpene called halomon, which is cytotoxic in nature ¹⁶. The Codium iyengarii is a potential source of steroidal glycosides known as iyengarosides A and B ¹⁷. Sargassum carpophyllum is the source of two bioactive sterols. Which induces morphological abnormality in the plant pathogenic fungus (Pyricularia oryzae) and exhibits cytotoxic activity against several cultured cancer cell lines ¹⁸. Laminaria and Sargassum species are used in China for the treatment of cancer. Undaria contains antiviral compounds which inhibit the herpes simplex virus. Corralina species are rich sources of calcium carbonate and hence are used in bone replacement therapies ¹⁹. Brown seaweeds produce terpenoids, acetogenins, and other aromatic compounds ^{20, 21, 22, 23, 24}.

Macroalgae from temperate and polar regions produce high concentrations of polyphenols called phlorotannins ^{25, 26}. Isoprenoid and acetogenin derivatives recognized from red seaweeds are useful as defensive metabolites ^{27, 28}. Bryopsidales are probable sources of sesquiterpenoid and diterpenoid compounds ²⁴. Several marine secondary metabolites have antifouling strategies due to their capability to inhibit the growth, attachment, and settlement of other marine organisms ^{29, 30, 31}. Seaweed extracts are being used for the treatment of asthma, thyroid, goiter, urinary infections, stomach ulcers, and even tumors. Sulfated polysaccharides such as carrageenan, agar, agarose, and furcellaran have wide applications in medicines. Carrageenan obtained from Chondrus, Eucheuma, Gigartina, and Iridea has an effective therapy for gastric and duodenal ulcers ^{32, 33}. Fucoidan obtained from Gracilaria corticata, is used for colorectal and breast cancer treatments ³⁴. L-kainic acid obtained from Digenea simplex is used in treatments of cancer, inflammation, and infectious diseases ³⁵. Phenolic compounds produced by Rhodomela confervoides, Symphyocladia latiuscula and Polysiphonia urceolata have antidiabetic activity. They inhibit the activity of protein tyrosine phosphatase (PTPase), which is a responsive factor for insulin. Polyphenolic compounds obtained from Laurencia undulate used for the treatment of asthma ³⁶.

Fucoxanthin obtained from macroalgae (Undaria pinnatifida, Laminaria japonica, Sargassum fulvellum, and Hijikia fusiformis) has antioxidant, anticancer, antiobesity, antidiabetic, and antiphotoaging activities ³⁷. Anticancer activity against several cell lines was observed from extracts of two Sargassum species (Sargassum wightii and Sargassum ilicifolium) ³⁸. Laminarin has strong heparin-like activity which is useful as an anticoagulant, antilipemic, antiviral, and anti-inflammatory agent ³⁹. Park et al. (2011) ⁴⁰ suggested that fucoidan can be used in obesity therapies as it reduces lipid accumulation by stimulating lipolysis. Spavieri (2010) ⁴¹ observed cytotoxic activity of twenty-one brown algae extract on mycobacteria and protozoan species. Fucoidans obtained from brown seaweed species have immune-modulating activity, which increases macrophage-mediated responses ⁴². Salgado suggested that the interaction between polyphenolic compounds and cell wall alginates leads to the absorption of ultraviolet radiation ⁴³. diekol obtained from Ecklonia cava has antifungal, anti-inflammatory, and antitype II diabetes activities ⁴⁴. Green seaweeds are rich sources of antioxidants, vitamins, and bioactive peptides ^{45, 46}. Extracts from Caulerpa taxifolia, Caulerpa racemose, and Cladophora pinnulata have hypotensive activities ⁴⁷. Sulfated polysaccharides from green seaweeds have anticoagulant, antioxidant, anticancer, anti-hyperlipidemic, and immune modulation activity ^{48, 49}. Sulfated polysaccharide obtained from Ulva pertusa is used for the treatment of ischemic, cerebrovascular, and cardiovascular diseases ⁵⁰.

Sulfated polysaccharides from Ulva pertusa, Capsosiphon fulvescens, and Codium fragile have immune-modulating activity for stimulating macrophages ⁵¹. The ethanolic extracts of Codium tomentosum have antigenotoxic and antioxidant activity ⁵². Ethanolic extract from Codium decorticatum has antibacterial activity ⁵³. The methanolic extract of Ulva linza has high inhibitory activity against inflammatory response due to the presence of high polyunsaturated fatty acids (PUFA) ⁵⁴.

MATERIALS AND METHODS:

Sample Collection: The six different macroalgae species (Ulva lactuca, Ulva faciata, Acanthophora dendroides, Gracilaria corticata, Padina tetrastromatica, and Cystoseira indica) were collected from the coastal region of Veraval behind College of fisheries (GPS Location: 20’54’41N 70’21’01’E).

Extraction of Secondary Metabolites: Seaweeds were collected and washed thoroughly with distilled water to remove unwanted impurities and other debris. They were allowed to dry for few days under sunlight. After drying, each macroalgae species was cut into small pieces and made into a coarse powder with the help of a mechanical grinder. Dry powder from each algae (Ulva lactuca, Ulva faciata, Acanthophora dendroides, Padina tetrastromatica, Cystoseira indica, and Gracilaria corticata) was filled in a thimble and was subjected for extraction in a soxhlet extractor. Extraction was carried out in different solvents starting from nonpolar solvents (petroleum ether and n-hexane) to semi-polar solvents (chloroform and acetone) and finally polar solvents (methanol and water) at 70 °C using a soxhlet extractor. After extraction, samples of methanol extract were concentrated using a rota evaporator. Then, concentrated samples were subjected to LC-MS analysis for the characterization of secondary metabolites.

LC-MS/MS analysis of samples: Each Sample (10 µl) was run on a Shimadzu UHPLC system composed of two LC-20AD XR UHPLC pumps, a Shimadzu DGU-20A 5R degassing unit, a Shimadzu SIL-20A XR auto sampling unit, a Shimadzu SPD-N20A UV DAD detector equipped with a UHPLC cell, and a Shimadzu IT-TOF detector mounting an Electrospray source. A Reprosil-Pur Basic C18 (1.9 μm^–100 × 2.0 mm) column was mounted in the UHPLC system and fed at 0.25 ml min⁻¹ with solution made of 0.05 M NH4CH-3COO in LC–MS grade water (A) and in LC–MS grade acetonitrile (B) by the following gradient: 95:5 A:B  for 0.1 min; linear gradient to 80:20 in 10 min, then to 50:50 in 20 min and finally to 10:90 in 20 min. The system was kept at 10:90 for 5 min and then re-equilibrated to 95:5 in 10 min for a total of 65 min run cycle. The stationary phase was stabilized at 30 °C.

Data Acquisition and Processing: All LC-MS data were converted to the mzdata format. Data preprocessing was performed using MZmine 2.23. Fragmentations were gathered with the corresponding precursor ions. Precursor ions of the metabolites were identified by using the MET-LIN metabolite database (http://metlin.scripps.edu/).

RESULTS: In present studies, extraction and characterization of metabolites from six different macroalgae species were done to identify the different type of bioactive metabolites present in them. From, methanolic extract of Ulva lactuca totally five peaks were identified, which included amino acids (betaine, L-Methionine and L-Asparagine) and phytohormones (6-Benzylaminopurine and jasmonate) Fig. 1. From, methanolic extract of Ulva faciata totally seven peaks were identified, which included amino acids (L-arginin, L-Proline, L-histidine, L-valine, and L-threonine), vitamin (Dihydrofolic acid), and sugar (glucosamine) Fig. 2.

FIG. 1: CHROMATOGRAM OF ULVA LACTUCA METHANOL EXTRACT

Peak	Compound name	Ret. Time	Type of Compound
1	Betaine	5.774	aminoacid
2	L-Methionine	9.631	aminoacid
3	6-Benzylaminopurine	15.909	Phytohormone
4	jasmonate	16.888	Phytohormone
5	L-Asparagine	20.439	aminoacid

FIG. 2: CHROMATOGRAM OF ULVA FACIATA METHANOL EXTRACT

Peak	Compound name	Ret. Time	Type of compound
1	L-Arginine	6.053	aminoacid
2	L-Proline	9.973	aminoacid
3	Dihydrofolic acid	13.908	Vitamin B9
4	L-Histidine	16.454	aminoacid
5	glucosamine	19.531	sugar
6	L-Valine	24.381	aminoacid
7	L-Threonine	27.776	aminoacid

FIG. 3: CHROMATOGRAM OF ACANTHOPHORA DENDROIDES METHANOL EXTRACT

Peak	Compound name	Ret. Time	Type of compound
1	D-Xylose	5.359	Sugar
2	Nicotinic acid	9.121	vitamin B3
3	L-glutamic acid	13.139	Amino acid
4	D-mannose	14.611	Sugar
5	L-Alanine	15.800	Amino acid
6	L-Serine	16.894	Amino acid
7	L-phenylalanine	18.377	Amino acid
8	L-Tyrosine	19.903	Amino acid
9	D-Fructose	24.740	Sugar
10	L-Glycine	31.554	Amino acid

From, methanol extract of Acanthophora dendroides ten peaks were identified, which included six amino acids (L-glutamic acid, L-alanine, L-serine, L-phenylalanine, L-Tyrosine, and L-glycine), three sugars (D-xylose, mannose and D-fructose) and one vitamin (Nicotinic acid) Fig. 3. From methanol extract of Gracilaria corticata eight peaks were identified, which included three aminoacids (L-Canavanine, L-isoleucine and L-Cysteine), three sugars (D-Rhamnose, fucose and D-galactose) and two phytohormones (Salicylic acid and ethylene) Fig. 4.

FIG. 4: CHROMATOGRAM OF GRACILARIA CORTICATA METHANOL EXTRACT

Peak	Compound name	Ret. Time	Type of compound
1	D-Rhamnose	5.644	sugar
2	L-Canavanine	9.733	aminoacid
3	fucose	17.103	Sugar
4	Salicylic acid	18.497	Phytohormone
5	ethylene	20.460	Phytohormone
6	L-isoleucine	21.664	aminoacid
7	D-galactose	24.251	sugar
8	L-Cysteine	28.988	aminoacid

From methanol extract of Padiana tetrastromatica seven peaks were identified which contained compounds such as three aminoacids (L-Aspartic acid, L-Tyrosine, and L-Leucine), one vitamin (Pantothenic acid), two sugars (Glucuronic acid and D-Glucose), and one phytohormones (abscissic acid).  Aminoacids identified were L-aspartic acid, L-Tyrosine and L-leucine. Sugars identified were glucuronic acid and D-Glucose. Phytohormone identified was abscisic acid, and vitamin identified was Pantothenic acid Fig. 5. From methanol extract of Cystosera indica only four peaks were identified, which contained vitamin (pyridoxamine-5-phosphate), sugars (arabinose and maltose) and phytohormones (Indole 3-acetic acid) Fig. 6.

FIG. 5: CHROMATOGRAM OF PADIANA TETRASTROMATICA METHANOL EXTRACT

Peak	Compound name	Ret. Time	Type of compound
1	Pantothenic acid	2.671	Vitamin B5
2	D-Glucuronic acid	3.268	Sugar
3	D-Glucose	3.661	Sugar
4	Abscisic acid	14.044	Phytohormone
5	L-Aspartic acid	17.786	aminoacid
6	D-mannuronic acid	19.834	Sugar
7	L-Leucine	26.348	Amino acid

FIG. 6: CHROMATOGRAM OF CYSTOSERA INDICA METHANOL EXTRACT

Peak	Compound name	Ret. Time	Type of compound
1	Pyridoxamine-5-phosphate	3.717	Vitamine B6
2	arabinose	4.488	sugar
3	maltose	4.889	sugar
4	Indole-3 acetic acid	5.066	Phytohormone

DISCUSSION: From the present studies, it was observed that all algae species contained aminoacids, vitamins, sugars, and phytohormones. From methanolic extract of all six marine macroalgae amino acids such as betaine, L-methionine, L-asparagine, L-arginine, L-proline, L-histidine, L-valine, L-threonine,  L-glutamic acid, L-alanine, L-serine, L-phenylalanine, L-Tyrosine and L-Glycine, L-Canavanine, L-isoleucine, L-Cysteine, L-Aspartic acid, and L-Leucine were identified. Similarly, in previous studies, Ortiz et al. 2006 ⁵⁵ had reported the presence of seventeen aminoacids (asparagine, glutamate, serine, histidine, glycine, therionine, arginine, alanine, proline, tyrosine, valenine, methionine, cysteine, isoleucine, leucine, phenylalanine, and lysine) from Ulva lactuca collected from the coastal area of Northern Chile.

Garcia et al. 2016 ⁵⁶ reported the presence of fifteen amino acids (aspartic acid, threonine, serine, glutamic acid, lysine, arginine, glycine, phenylalanine, typtophan, methionine, cysteine, isoleucine, leucine, histidine, and valine) in four macroalgae (Ulva, Codium, Halymenia floresia, and Saccorhiza polyschides) collected from Barbate estuary, Gulf of Cadiz, Spain. Kumar and Kaladharan (2007) ⁵⁷ reported the presence of eighteen amino acids (asparagine, glutamate, serine, histidine, glycine, therionine, arginine, alanine, proline, tyrosine, valenine, methionine, cysteine, isoleucine, leucine, phenylalanine, tryptophan, and lysine) from G. corticata, H. musciformis, A. spicifera, S. wightii, U. lactuca and K. alvarezii collected from Thikkodi Thangasseri and Quilon of Kerala coast. Recently Kazir et al. 2019 ⁵⁸ reported the presence of seventeen amino acids (alanine, arginine, aspartic acid, cysteine, glutamic acid, glycine, histidine, isoleucine, leucine, lysine, methionine, phenylalanine, proline, serine, therionine, tyrosine, and valenine) in Ulva sp. and Gracilaria sp. cultivated at the seaweed unit of Israel Oceanographic and Limnological Research, Haifa, Israel.

Sugars and sugar acids identified from six marine algal species were glucosamine, D-xylose, D-mannose, D-fructose, D-rhamnose, fucose, D-galactose, D-glucose, D-glucuronic acid, D-mannuronic acid, arabinose, and maltose. Similarly, in previous studies, Aguilar-Briseño et al. 2015 ⁵⁹ suggested the presence of rhamnose, glucuronic acid, xylose, glucose and galactose in the dry powder of Ulva clathrata. Robin et al. (2017) ⁶⁰ suggested the presence of glucose, rhamnose, galactose, xylose arabinose, mannitol, fucose, and glucuronic acid in Ulva sp., Gracilaria sp., Padina pavonica, Cladophora pellucid, Galacxaura rugosa, and Nemalion helminthoides. Agili and Mohamed 2012 ⁶¹ reported the presence of six sugars (rhamnose, fucose, xylose, mannose, glucose, and galactose) in the polysaccharide of Padina pavonia.

Vitamins identified from methanol extract of six marine macroalgae were Pyridoxamine-5-phosphate, Dihydrofolic acid, Pantothenic acid, and Nicotinic acid. Similarly, previous studies by Jesmi et al. 2018 ⁶² suggested the presence of folic acid, riboflavin, pantothanic acid, niacin, vitamin A, vitamin B1, vitamin B12, vitamin C, vitamin D, and vitamin E in seaweeds. Pandithurai and Murugesan (2014) ⁶³ suggested the presence of these vitamins in brown marine algae Spatoglossum asperum. Rodrıguez Bernaldo de Quirós et al., 2004 ⁶⁴ suggested the presence of folic acid in Himanthalia elongata, Laminaria ochroleuca, Palmaria spp., Undaria pinnatifida, Porphyra spp. and Saccorhiza polychides. Rosemary et al. 2019 ⁶⁵ reported the presence of vitamin B1, vitamin B2, vitamin B3, vitamin B6, vitamin B9, and vitamin C, vitamin A, and vitamin E in G. corticata and G. edulis.

Phytohormones identified from methanol extract of six marine macroalgae were 6-benzylaminopurine, jasmonate, indole butyric acid, salicylic acid, ethylene, abscisic acid, and indole-3 acetic acid. Recently, Yalcın et al. 2019 ⁶⁶ suggested the presence of zeatin, benzylaminopurine, gibberellic acid, kinetin, indole-3 acetic acid, and abscissic acid in nine seaweeds (Cladostephus spongiosum f. verticillatum, Colpomenia sinuosa, Cystoseira barbata, Halopithys incurva, Gracilaria bursapastoris, Ellisolandia elongata, Polysiphonia scopulorum, Penicillus capitatus, and Flabellia petiolata). Prasad et al., 2010 ⁶⁷ reported the presence of indole-3 acetic acid (IAA), zeatin, and Giberellic acid in Kappaphycus alvarezii and Sargassum tenerrimum. He also reported the presence of indole-3-pyruvic acid (IPA), zeatin, and gibberellic acid in Gracilaria edulis. Gupta et al., 2011 ⁶⁸ reported the presence of IAA, indole-3-butyric acid (IBA), salicylic acid (SA), and abscissic acid (ABA) in four wild Ulva species and in laboratory cultured Monostroma oxyspermum. Yokoya et al., 2010 ⁶⁹ reported presence of indole acetic acid (IAA), Indole-Acetamide (IAM) and ABA in elevan Rhodophyceae species of Bangiales, Gelidiales, Gracilariales and Gigartinales. Duan et al., 1995 ⁷⁰ reported the presence of zeatin in L. japonica. Stirk et al., 2009 ⁷¹ reported presence of ABA in Ulva fasciata and D. humifusa. Plettner et al., 2005 72 reported ethylene production by Ulva intestinalis. García-Jiménez et al., 2013 ⁷³ also reported ethylene production by Gelidium arbuscula.

CONCLUSION: From the above analysis, it was concluded that the bioactive compounds identified in the methanolic extract of six algae extracts were aminoacids, vitamins, sugars, and phytohormones. The aminoacids and vitamins present in Ulva lactuca, Ulva faciata, Acanthophora dendroides, Gracilaria coeticata, and Padina tetrastromatica can be utilized for the development of dietary supplements and proteinaceous food for domestic animals. The sugar present in Ulva faciata, Acanthophora dedroides, Gracilaria corticata, Padina tetrastromatica and Cystosera indica can be utilized in food products, cosmetics, gelling and thickening agents. The phytohormones present in Ulva lactuca, Gracilaria corticata, Padina tetrastromatica, and Cystosera indica can be utilized in agriculture as plant growth regulators. Hence, these algae species are essential raw materials for the production of various pharmaceutical and biotechnological products.

ACKNOWLEDGEMENT: Authors are heartily thankful to the Department of Biosciences, Saurashtra University, Rajkot for providing facilities to carry out present research work.

CONFLICTS OF INTEREST: Authors declare that there is no conflict of interest regarding the publication of this research article in the Journal

REFERENCES:

1. Rengasamy KR, Mahomoodally MF, Aumeeruddy MZ, Zengin G, Xiao J and Kim DH: Bioactive compounds in seaweeds: An overview of their biological properties and safety. Food and Chemical Toxicology 2020; 135: 111013.
2. Rotter A, Barbier M, Bertoni F, Bones AM, Cancela ML, Carlsson J, Carvalho MF, Cegłowska M, Chirivella-Martorell J, Conk Dalay M and Cueto M: The essentials of marine biotechnology. Frontiers in Marine Sci 202; 8: 158.
3. Bilal M and Iqbal HM: Biologically active macro-molecules: Extraction strategies, therapeutic potential and biomedical perspective. International Journal of Biological Macromolecules 2020; 151: 1-8.
4. Abbas MU, Saeed FA and Suleria HA: Marine bioactive compounds: Innovative trends in food and medicine. Plant-and Marine-Based Phytochemicals for Human Health: Attributes, Potential, and Use 2018; 61.
5. Al-Saif SSA, Abdel-Raouf N, El-Wazanani HA and Aref IA: Antibacterial substances from marine algae isolated from Jeddah coast of Red sea. Saudi Journal of Biological Sciences 2014; 21(1): 57-64.
6. Salem WM, Galal H and Nasr El-deen F: Screening for antibacterial activities in some marine algae from the red sea (Hurghada, Egypt). African Journal of Microbiology Research 2011; 5(15): 2160-67.
7. Rosa GP, Tavares WR, Sousa P, Seca AM and Pinto DC: Seaweed secondary metabolites with beneficial health effects: An overview of successes in in vivo studies and clinical trials. Marine Drugs 2020; 18(1): 8.
8. Selvin J and Lipton AP: Biopotentials of Ulva fasciata and Hypnea musciformis collected from the Peninsular Coast of India. J of Marine Science and Techn 2004; 12: 1-6.
9. Thirumurugan D, Cholarajan A, Raja SS and Vijayakumar R: An introductory chapter: secondary metabolites. Second metab-sources Appl 2018; 5: 1-21.
10. Bhattacharjee ME. Pharmaceutically valuable bioactive compounds of algae. Asi J Pharm Clin Res 2016; 9: 43-7.
11. El-Beltagi HS, Mohamed HI and Abou El-Enain MM: Role of Secondary Metabolites from Seaweeds in the Context of Plant Development and Crop Production. InSeaweeds as Plant Fertilizer, Agricultural Biostimulants and Animal Fodder CRC Press 2019; 64-79.
12. Janarthanan M and Senthil Kumar M: The properties of bioactive substances obtained from seaweeds and their applications in textile industries. Journal of Industrial Textiles 2018; 48(1): 361-01.
13. Garg HS, Sharma T, Bhakuni DS, Pramanik BN and Bose AK: An antiviral sphingosine derivative from green alga Ulva fasiata, Tetrahedron Letters 1992; 33: 1641-44.
14. Arsianti A, Wibisono LK, Azizah NN, Putrianingsih R, Murniasih T, Rasyid A and Pangestuti R: Phytochemical composition and anticancer activity of seaweeds Ulva lactuca and Eucheuma cottonii against breast MCF-7 and colon HCT-116 cells. Asian Journal of Pharmaceutical and Clinical Research 2016; 1: 115-9.
15. Lipton M and Zhang Qi: Reducing poverty and inequality during liberalisation in China: Rural and agricultural experiences and policy options’. In Changing Contours of Asian Agriculture: essays in honour of Professor V. S. Vyas (Eds Surjit Singh and V. Ratna Reddy). Delhi: Academic Foundation with Jaipur: Inst Development Studies 2009
16. Knott MG: An examination of the chemical structures and in-vitro cytotoxic bioactivity of halomon related secondary metabolites from Portieria hornemannii found worldwide. International Science and Technology Journal of Namibia. 2017; 28: 15-30.
17. Ivanchina NV, Kicha AA and Stonik VA: Steroid glycosides from marine organisms. Steroids 2011; 76(5): 425-54.
18. Jha RK and Zi-Rong X: Biomedical compounds from marine organisms. Marine Drugs 2004; 2(3): 123-46.
19. Wilson B and Hayek LA: Calcareous meiofauna associated with the calcareous alga Corallina officinalis on bedrock and boulder-field shores of Ceredigion, Wales, UK. Journal of the Marine Biological Association of the United Kingdom 2020; 100(8): 1205-17.
20. Qasim R: Amino acid composition of some common seaweeds. Pakistan J of Pharm Sciences 1991; 4: 49-54.
21. Young RM, Schoenrock KM, von Salm JL, Amsler CD and Baker BJ: Structure and function of macroalgal natural products. InNatural products from marine algae 2015 (pp. 39-73). Humana Press, New York, NY.
22. Trius A and Sebranek JG: Carrageenans and Their Use in Meat Products. Critical Reviews in Food Science and Nutrition 1996; 36(1-2): 69-85.
23. El Gamal AA: Biological importance of marine algae. Saudi Pharmaceutical Journal, 2010; 18(1): 1-33.
24. Blunt JW, Copp BR, Munro MHG, Northcote PT, Prinsep MR (2011). Marine natural products. Nat Prod Rep 2011; 28: 196-68.
25. Flores‐Molina MR, Rautenberger R, Munoz P, Huovinen P and Gomez I: Stress tolerance of the endemic antarctic brown alga Desmarestia anceps to UV radiation and temperature is mediated by high concentrations of phlorotannins. Photochemistry and photobiology. 2016; 92(3): 455-66.
26. Le Lann K, Surget G, Couteau C, Coiffard L, Cérantola S, Gaillard F, Larnicol M, Zubia M, Guérard F, Poupart N, Stiger-Pouvreau V. Sunscreen, antioxidant, and bactericide capacities of phlorotannins from the brown macroalga Halidrys siliquosa. J of App Phycol 2016; 28(6): 3547-59.
27. Parkavi K, Raja R, Arunkumar K, Coelho A, Hemaiswarya S and Carvalho IS: Recent insights into algal biotechnology: an update using text mining tool. Encyclopedia of Marine Biotechnology 2020; 1: 569-84.
28. Harper MK, Bugni TS, Copp BR, James RD, Lindsay BS, Richardson AD, Schnabel PC, Tasdemir D, VanWagoner RM, Verbitski SM and Ireland CM: Introduction to the chemical ecology of marine natural products. In: McClintock JB, Baker BJ (org.). Marine chemical ecology. ed. Boca Raton: CRC Press 2001; 3-79.
29. Hellio C, Thomas-Guyon H, Culioli G, Piovetti L, Bourgougnon N and Le Gal Y: Marine antifoulants from Bifurcaria bifurcata (Phaephyceae, Cystoseiraceae) and other brown macroalgae. Biofouling 2001; 17: 189-201.
30. Fusetani N Biofouling and antifouling. Nat Prod Rep 2004; 21: 94-104.
31. Qian PY, Xu Y and Fusetani N: Natural products as antifouling compounds: recent progress and future perspectives. Biofouling 2010; 26: 223-34.
32. Kamath V and Pai A: A review on marine natural products and their application in modern medicine. International Journal of Green Pharmacy (IJGP) 2018; 12(01): S46-S50.
33. Prajapati VD, Maheriya PM, Jani GK and Solanki HK: Carrageenan: A natural seaweed polysaccharide and its applications. Carbohydr. Polym 2014; 105: 97-12.
34. Deepa S, Bhuvana B, Hemamalini S, Janet C, Kumar S: Therapeutic potential and pharmacological significance of the marine algae Gracilaria corticata. Pharm Biol Eval 2017; 4: 68-72.
35. Swargiary A: Recent trends in traditionally used medicinal plants and drug discovery. Asian Journal of Pharmacy and Pharmacology 2017; 3(4): 111-20.
36. Collins KG, Fitzgerald GF, Stanton C and Ross RP: Looking beyond the terrestrial: The potential of seaweed derived bioactives to treat non-communicable diseases. Mar. Drugs 2016; 14: 60.
37. D’Orazio N, Gemello E, Gammone MA, de Girolamo M, Ficoneri C and Riccioni G: Fucoxantin: A treasure from the sea. Mar Drugs 2012; 10: 604-16
38. Yende SR, Harle UN and Chaugule BB: Therapeutic potential and health benefits of Sargassum species. Pharmacognosy Reviews. 2014; 8(15):1.
39. Barzkar N, Jahromi ST, Poorsaheli HB and Vianello F: Metabolites from marine microorganisms, micro, and macroalgae: immense scope for pharmacology. Marine Drugs 2019; 17(8):464.
40. Park MK, Jung U and Roh C: Fucoidan from marine brown algae inhibits lipid accumulation. Mar Drugs 2011; 9: 1359-67.
41. Spavieri J, Allmendinger A, Kaiser M, Casey, R, Hingley Wilson S, Lalvani A, Guiry MD, Blunden G and Tasdemir D: Antimycobacterial, antiprotozoal and cytotoxic potential of twenty-one brown algae (phaeophyceae) from british and irish waters. Phytother Res 2010; 24: 1724-29
42. Hsu HY and Hwang PA: Clinical applications of fucoidan in translational medicine for adjuvant cancer therapy. Clinical and Translational Medicine 2019; 8(1): 1-8.
43. Salgado LT, Tomazetto R, Cinelli LP, Farina M and Amado Filho GM: The influence of brown algae alginates on phenolic compounds capability of ultraviolet radiation absorption in-vitro. Braz J Oceanogr 2007; 55: 145-54.
44. Kang MC, Wijesinghe W, Lee SH, Kang SM, Ko SC, Yang X, Kang N, Jeon BT, Kim J and Lee DH: Dieckol isolated from brown seaweed Ecklonia cava attenuates type iidiabetes in db/db mouse model. Food Chem. Toxicol 2013; 53: 294-98.
45. Cho M, Lee HS, Kang IJ, Won MH and You S: Antioxidant properties of extract and fractions from Enteromorpha prolifera, a type of green seaweed. Food Chem 2011; 127: 999-06.
46. Lafarga T, Acién-Fernández FG and Garcia-Vaquero M: Bioactive peptides and carbohydrates from seaweed for food applications: Natural occurrence, isolation, puri-fication, and identification. Algal Res 2020; 48: 101909.
47. Barzkar N, Jahromi ST, Poorsaheli HB and Vianello F: Metabolites from marine microorganisms, micro, and macroalgae: immense scope for pharmacology. Marine Drugs 2019; 17(8): 464.
48. Cho M and You S: Sulfated polysaccharides from green seaweeds. InSpringer Handbook of Marine Biotechnology. Springer, Berlin, Heidelberg 2015; 941-953.
49. Hickey RM: Extraction and characterization of bioactive carbohydrates with health benefits from marine resources: Macro-and microalgae, cyanobacteria, and invertebrates. In Marine Bioactive Compounds; Springer: Boston, MA, USA 2012; 159-72.
50. Pengzhan Y, Quanbin Z, Ning L, Zuhong X, Yanmei W, Zhien L: Polysaccharides from Ulva pertusa (chlorophyta) and preliminary studies on their antihyperlipidemia activity. J Appl phycol 2003; 15: 21–27.
51. Tabarsa M, Lee SJ and You S: Structural analysis of immunostimulating sulfated polysaccharides from Ulva pertusa. Carbohydr Res 2012; 361: 141-47.
52. Celikler S, Vatan O, Yildiz G and Bilaloglu R: Evaluation of anti-oxidative, genotoxic and antigenotoxic potency of Codium tomentosum Stackhouse ethanolic extract in human lymphocytes in-vitro. Food and Chemical Toxicology 2009; 47(4): 796-801.
53. Sunilson JAJ, Suraj R, Anandarajagopal K, Rejitha G, Vignesh M and Promwichit P: Preliminary phytochemical analysis, elemental determination and antibacterial screening of Codium decorticatum - A marine green algae. Int J Biol Chem 2009; 3: 84-89.
54. Khan MN, Choi JS, Lee MC, Kim E, Nam TJ, Fujii H and Hong YK: Anti-inflammatory activities of methanol extracts from various seaweed species. J Environ Biol 2008; 29: 465-69.
55. Ortiz J, Romero N, Robert P, Araya J, Lopez-Hernández J, Bozzo C, Navarrete E, Osorio A and Rios A: Dietary fiber, amino acid, fatty acid and tocopherol contents of the edible seaweeds Ulva lactuca and Durvillaea antarctica. Food Chemistry 2006; 99(1): 98-104.
56. Garcia JS, Palacios V and Roldán A: Nutritional Potential of Four Seaweed Species Collected in the Barbate Estuary (Gulf of Cadiz, Spain). J Nutr Food Sci 2016; 6: 505.
57. Kumar VV and Kaladharan P: Amino acids in the seaweeds as an alternate source of protein for animal feed. J of the Marine Biol Associat of India 2007; 49(1): 35-40.
58. Kazir M, Abuhassira Y, Robin A, Nahor O, Luo J, Israel A, Golberg A and Livney YD: Extraction of proteins from two marine macroalgae, Ulva sp. and Gracilaria sp., for food application, and evaluating digestibility, amino acid composition and antioxidant properties of the protein concentrates. Food Hydrocolloids 2019; 87: 194-03.
59. Aguilar-Briseño JA, Cruz-Suarez LE, Sassi JF, Ricque-Marie D, Zapata-Benavides P, Mendoza-Gamboa E, Rodríguez-Padilla C and Trejo-Avila LM: Sulphated polysaccharides from Ulva clathrata and Cladosiphon okamuranus seaweeds both inhibit viral attachment/entry and cell-cell fusion, in NDV infection. Marine drugs. 2015; 13(2): 697-12.
60. Robin A, Chavel P, Chemodanov A, Israel A and Golberg A: Diversity of monosaccharides in marine macroalgae from the Eastern Mediterranean Sea. Algal Research 2017; 28: 118-27.
61. Agili FA and Mohamed SF: Polysaccharides from Padina pavonia: Chemical structural and antioxidant activity. Australian J of Basic and App Sci 2012; 6(5): 277-83.
62. Jesmi D, Viji P and Rao BM: Seaweeds: A promising functional food ingredient. Visakhapatnam Research Centre of ICAR-Central Institute of Fisheries Technology 2018.
63. Murugesan PMS: Biochemical composition of brown marine alga Spatoglossum asperum. J Chem Pharm Res 2014; 6: 133-7.
64. De Quirós AR, De Ron CC, Lopez-Hernandez J and Lage-Yusty MA: Determination of folates in seaweeds by high-performance liquid chromatography. Journal of Chromatography A 2004; 1032(1-2): 135-9.
65. Rosemary T, Arulkumar A, Paramasivam S, Mondragon-Portocarrero A and Miranda JM: Biochemical, micronutrient and physicochemical properties of the dried red seaweeds Gracilaria edulis and Gracilaria corticata. Molecules 2019; 24(12): 2225.
66. Yalçın S, Şükran Okudan E, Karakaş Ö, Önem AN and Sözgen BK: Identification and quantification of some phytohormones in seaweeds using UPLC-MS/MS. Journal of Liq Chromato & Rela Techno 2019; 42(15-16): 475-84.
67. Prasad K, Das AK, Oza MD, Brahmbhatt H, Siddhanta AK, Meena R, Eswaran K, Rajyaguru MR and Ghosh PK: Detection and quantification of some plant growth regulators in a seaweed-based foliar spray employing a mass spectrometric technique sans chromatographic separation. Journal of Agricultural and Food chemistry. 2010; 58(8): 4594-01.
68. Gupta V, Kumar M, Brahmbhatt H, Reddy CR, Seth A and Jha B: Simultaneous determination of different endogenetic plant growth regulators in common green seaweeds using dispersive liquid–liquid microextraction method. Plant Physio and Biochem 2011; 49(11): 1259-63.
69. Yokoya NS, Stirk WA, Van Staden J, Novák O, Turečková V, Pěnčí KA and Strnad M: endogenous cytokinins, auxins, and abscisic acid in red algae from Brazil. Journal of Phycology 2010; 46(6): 1198-05.
70. Duan D, Liu X, Pan F, Liu H, Chen N and Fei X: Extraction and identification of cytokinin from Laminaria japonica Aresch. Botanica Marina 1995; 38(1-6): 409-12.
71. Stirk WA, Novák O, Hradecká V, Pĕnčík A, Rolčík J, Strnad M and Van Staden J: Endogenous cytokinins, auxins and abscisic acid in Ulva fasciata (Chlorophyta) and Dictyota humifusa (Phaeophyta): towards understanding their biosynthesis and homoeostasis. European Journal of Phycology 2009; 44(2): 231-40.
72. Plettner IN, Steinke M, Malin G. Ethene (ethylene) production in the marine macroalga Ulva (Enteromorpha) intestinalis L.(Chlorophyta, Ulvophyceae): effect of light stress and co‐production with dimethyl sulphide. Plant, Cell & Environment. 2005; 28(9): 1136-45.
73. Garcia Jimenez P, Brito Romano O and Robaina RR. Production of volatiles by the red seaweed Gelidium arbuscula (Rhodophyta): emission of ethylene and dimethyl sulfide. Journal of Phycology 2013; 49(4): 661-9.
    

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    How to cite this article:

    Goswami HP, Tank JG and Pandya RV: Characterization of bioactive metabolites from marine macroalgae collected from veraval coast of Gujarat. Int J Pharm Sci & Res 2022; 13(1): 173-80. doi: 10.13040/IJPSR.0975-8232.13(1).173-80.

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